Rats Fed a Diet Rich in Fats and Sugars Are Impaired in the Use of Spatial Geometry

Abstract

A diet rich in fats and sugars is associated with cognitive deficits in people, and rodent models have shown that such a diet produces deficits on tasks assessing spatial learning and memory. Spatial navigation is guided by two distinct types of information: geometrical, such as distance and direction, and featural, such as luminance and pattern. To clarify the nature of diet-induced spatial impairments, we provided rats with standard chow supplemented with sugar water and a range of energy-rich foods eaten by people, and then we assessed their place- and object-recognition memory. Rats exposed to this diet performed comparably with control rats fed only chow on object recognition but worse on place recognition. This impairment on the place-recognition task was present after only a few days on the diet and persisted across tests. Critically, this spatial impairment was specific to the processing of distance and direction.

Keywords

diet object-recognition memory spatial memory geometric processing

Many people in Western societies eat a diet rich in saturated fat and refined carbohydrates. It has long been recognized that excessive intake of energy-rich foods is associated with metabolic disorders, cardiovascular disease, and certain cancers (Eckel, Grundy, & Zimmet, 2005; Haslam & James, 2005). More recent evidence indicates that excessive intake of energy-rich foods is also associated with cognitive impairments in children (Li, Dai, Jackson, & Zhang, 2008), adolescents (Nyaradi et al., 2014; Overby, Ludemann, & Hoigaard, 2013), and the elderly (Anstey, Lipnicki, & Low, 2008; Kalmijn et al., 1997). Moreover, a few days of exposure to a high-fat diet was sufficient to impair the performance of healthy adult volunteers in tasks measuring attention and memory retrieval (Edwards et al., 2011; Holloway et al., 2011).

Studies with rodents have confirmed that extended exposure to a high-fat, high-sugar, or both high-fat and high-sugar (HFHS) diet impairs performance on tasks assessing hippocampal-dependent spatial learning and memory, such as those requiring the use of extramaze cues to navigate to a hidden platform in the Morris water maze or the avoidance of arms that have been visited and depleted of food in arm mazes (Jurdak, Lichtenstein, & Kanarek, 2008; Kanoski, Meisel, Mullins, & Davidson, 2007; Molteni, Barnard, Ying, Roberts, & Gomez-Pinilla, 2002; Pistell et al., 2010; Ross, Bartness, Mielke, & Parent, 2009; Ross, Darling, & Parent, 2013; Valladolid-Acebes et al., 2011). There is also evidence that exposure to energy-rich diets for a few days is sufficient to produce impairments in the radial-arm maze (Kanoski & Davidson, 2010; A. J. Murray et al., 2009) and a place-recognition task (Beilharz, Maniam, & Morris, 2014).

However, the nature of the spatial deficit produced by energy-rich diets remains unclear. In the series of experiments reported here, we fed rats a diet containing energy-rich foods eaten by people and assessed their performance in place- and object-recognition tasks. The aims were to examine the conditions under which a deficit on the place task occurred and to determine whether this deficit was specific to the use of geometrical (e.g., distance and direction) or featural (e.g., luminance and pattern) information. The initial experiments showed that the energy-rich diet produced a rapid and persistent impairment specific to place recognition. Subsequent experiments showed that the provision of featural cues ameliorated the impairment in place recognition, which indicates that the impairment involved processing geometrical information. The final experiment used a distinctively cued rectangular environment to confirm that rats fed the energy-rich diet used features rather than geometry, whereas control rats fed only on chow used geometry rather than features.

Experiments 1 and 2

Experiments 1 and 2 examined the effects of an HFHS diet on a hippocampal-dependent task requiring place-recognition memory (Mumby, Gaskin, Glenn, Schramek, & Lehmann, 2002) and a perirhinal-dependent task requiring object-recognition memory (E. A. Murray & Richmond, 2001). Our aim in both experiments was to replicate and extend recent findings that an energy-rich diet impairs place but not object recognition.

Method

Subjects

Subjects were 32 male Sprague-Dawley rats that had not previously been used in an experiment. Rats were obtained from a commercial supplier (Animal Research Centre, Perth, Western Australia, Australia) and weighed between 200 and 300 g on arrival in the laboratory. They were housed in plastic tubs (width = 65 cm, length = 40 cm, height = 32 cm) in a climate-controlled colony room (lights on from 7:00 a.m. to 7:00 p.m.). There were 4 rats in each tub. Rats were handled for 2 to 3 min each day over at least 5 days prior to testing. All procedures were approved by the Animal Ethics Committee, University of New South Wales.

Diet

The diet for chow rats consisted of ad libitum access to water and standard laboratory chow (Premium Rat and Mouse Breeder’s Diet, Gordon’s Specialty Stock Feeds, Yanderra, New South Wales, Australia), which has a nutrient breakdown of 25% protein, 15% fat, 55% complex carbohydrates, and 5% sugar. In addition to the standard chow and water, HFHS rats had access to a 10% sucrose solution and also received lard and a range of supermarket foods (various types of cakes and biscuits), which were replaced daily. This diet provided an average nutrient breakdown of 5% protein, 40% fat, 15% complex carbohydrates, and 40% sugar. Although the HFHS diet contained a much smaller percentage of energy from protein compared with the control diet, HFHS rats consumed a greater amount of total energy. As a result, the protein intake of rats from both groups, on average, was equivalent (see the Supplemental Material available online).

Apparatus

The place- and object-recognition-memory tasks were conducted in a square arena (width = 60 cm, length = 60 cm, height = 50 cm) constructed out of wood and coated with oil-based paint. The walls of this arena were uniformly black. The objects used were commercially available household items (maximum volume: width = 10 cm, length = 10 cm, height = 20 cm) that varied in material, texture, and shape (e.g., tin cans, plastic bottles, glass jars; see the Supplemental Material available online). Items with a lid were emptied, washed, and cleaned before use, and there were three copies of each object (two were used for the place task and three were used for the object task). Black curtains surrounded the arena, and a camera was mounted approximately 1.85 m above the arena floor for recording the rat’s behavior. A small home cage (width = 40 cm, length = 30 cm, height = 30 cm) filled with bedding was used to hold the rats between the two phases (familiarization and test) of each place and object trial.

Procedure

Each rat was exposed to the arena for 10 min each day over 2 days. A baseline test of place- and object-recognition memory occurred over 2 days immediately following context familiarization and immediately before the start of the dietary manipulation. Testing on the place and object task was always counterbalanced, with half of the rats in each diet condition tested on the place task on the 1st day and the object task on the 2nd day; this order remained the same across repeated tests for any given rat. The first retest occurred 7 days after the baseline test, and retesting was repeated weekly three times while the rats were fed their respective diets.

Place-recognition trials involved putting the rat into the arena with two identical objects (see Fig. 1). The rat was allowed to explore the arena and objects during this familiarization phase for 5 min. The rat was then removed from the arena and placed in the holding cage for a retention interval of 5 min. During this time, the arena and objects were cleaned with a 70% ethanol solution. The rat was then returned to the arena with one object in the same location and the other object in a new location. The rat was allowed to explore the arena and objects during this test phase for 3 min.

Fig. 1.

Diagrams illustrating the design of the place- and object-recognition tasks. In Experiment 1 (a), two objects were placed in the center of the arena during the familiarization phase. At test, one of the objects either had been moved to a corner of the arena (place trials) or had been swapped with a different object in the same location (object trials). In Experiment 2 (b), two objects were placed in separate corners during the familiarization phase of place trials, and at test, one had been moved to a center location; in object trials, one object was in a corner and the other was in the center during the familiarization phase, and at test, the center object had been swapped with a different object in the same location. In both experiments, there was a 5-min retention interval between familiarization and test.

Object-recognition trials were identical to place-recognition trials except at test (see Fig. 1). For object trials, the object locations were maintained when the rat was returned to the arena. However, one object was an identical replica of the objects presented during the familiarization phase, while the other object was novel. Across repeated tests, rats were presented with a different set of objects, and object locations cycled through four different spatial layouts in the arena before repeating. Object sets and object locations were counterbalanced between groups and across repeated tests.

Experiments 1 and 2 differed in the layout of the objects in the arena. Experiment 1 used a novel-corner-location variant of the task (Fig. 1a): In place trials, both objects were in the center of the arena during familiarization, but one was moved to a corner of the arena for the test. Experiment 2 used a novel-center-location variant of the task (Fig. 1b): In place trials, both objects were placed in the corners of the arena during familiarization, but one was moved to the center of the arena for the test. (On object trials, the locations of objects did not change between familiarization and test, but in Experiment 1, both objects were in the center of the arena, whereas in Experiment 2, one object was in a corner and one object was in the center.) These two location variants are important because they mutually rule out the possibility that any between-groups differences in novelty preference on the place task are due to differences in preference for or aversion to arena locations, such as the walls or center. Novelty preference was used as an index of place- and object-recognition memory. Novelty preference was quantified as the time spent exploring the novel place or novel object divided by the total time spent exploring both objects: time_novel /(time_novel + time_familiar). Exploration was defined as directly facing the object and making contact by brushing the object with whiskers or sniffing it. Rearing, climbing, or sitting on the object was not scored as exploration.

Analysis

Place trials were selected equally across diet conditions and all repeated tests to be cross-scored. Every rat was selected at least once, and this resulted in a minimum of 25% place trials from each experiment being scored by two observers. Interrater reliability was greater than .90 for each experiment, and there were no trials for which scores differed by more than 10%.

Test trials were excluded from statistical analysis when an object was knocked over and remained that way for more than 30 s (if the object was picked up and placed in its designated location by the experimenter, the trial was included, but exploration during this time was not counted). Test trials were also excluded when a rat jumped out from the base of the arena onto the edge of the arena walls and remained there for more than 30 s, a rat made one or less instances of exploratory contact with an object, or an object was placed in the incorrect location.

Excluded test trials were never exclusive to any one diet condition in either experiment. Missing values from excluded trials were replaced with the rat’s average score from the two closest trials, where appropriate. Details about the number of excluded rats and the test trials they were excluded from can be found in the Supplemental Material.

Results

HFHS rats consumed more and weighed more than chow rats (see Figs. S2 and S3 in the Supplemental Material). HFHS rats exhibited an equal novelty preference on the object task as chow rats but a lower novelty preference on both the novel-corner (Experiment 1; Figs. 2a–2d) and novel-center (Experiment 2; Figs. S4a–S4d in the Supplemental Material, which also includes the results of statistical analyses for Experiment 2) variants of the place task. In Experiment 1, analyses on the place task revealed a significant effect of diet, F(1, 30) = 9.00, p = .005, η_p² = .23, and no effect of repeated tests, F(2, 60) = 1.33, or interaction between the two factors, F(2, 60) = 0.18; for the object task, there was no effect of diet or repeated tests, F(2, 60) = 1.23, and no interaction (Fs < 1). Notably, the differences in the time spent exploring the object moved to the novel location in either the corner or center were not due to differences in the total amount of time spent exploring; the two groups spent an equivalent amount of time exploring but differed in how this time was distributed (Figs. 2e and 2f for the novel-corner task; Figs. S4e and S4f for the novel-center task). In Experiment 1, there was no effect of diet or repeated tests in the place task, nor an interaction, Fs < 1; for the object task, there was a significant effect of repeated tests, F(2, 60) = 4.24, p = .02, η_p² = .12, but this was comparable between the diet conditions, and there was no interaction between diet and repeated tests, Fs < 1.

Fig. 2.

Results from the place-recognition task (top row) and object-recognition task (bottom row) in Experiment 1. The mean proportion of trials on which rats explored (a, b) is shown as a function of diet day and group. These results are also shown collapsed across days for each group (c, d). Mean exploration time (e, f) is shown as a function of diet day and group. The dotted lines in (a) through (d) indicate chance performance. Error bars indicate +1 SEM. HFHS = high-fat, high-sugar.

Discussion

Rats fed the HFHS diet performed comparably with those fed chow on the object task but worse on the place task. Furthermore, this difference in performance was (a) independent of the locations occupied by the objects in the arena, (b) present after 5 days on the diet when body weights were similar and on subsequent tests when body weights had diverged, and (c) not due to differences in task motivation.

Experiments 3 and 4

Experiments 3 and 4 examined the effect of the HFHS diet on place-recognition memory when the arena was enriched with spatial information: black-and-white-striped walls. The question of interest was whether HFHS rats would show the same deficit in place recognition when provided with featural cues such as striped walls. If the HFHS diet causes a global impairment in spatial processing, then performance of HFHS rats in a featurally cued arena will remain poor relative to chow rats. However, if the HFHS diet causes a selective impairment in geometrical processing, then the addition of featural cues will improve performance.

Method

Subjects

Subjects were 32 rats of the same sex and strain as in Experiments 1 and 2. Rats were from the same supplier and were kept under the same conditions. None had performed in previous experiments, and all weighed between 200 and 300 g on arrival.

Apparatus

The same square arena used in Experiments 1 and 2 was used in Experiment 3. Experiment 4 used a square arena (width = 60 cm, length = 60 cm, height = 65 cm) constructed of black Perspex. In addition to the standard arena, a cued arena was used in Experiments 3 and 4, and a scrambled arena was added in Experiment 4. For the cued and scrambled arenas, Perspex panels were attached to the inside of the standard arena, completely covering the walls.

The cued arena contained two vertically striped black (B) and white (W) panels (one WBWB and the other BWBW from left to right) and two horizontally striped black and white panels (one WBWB and the other BWBW from top to bottom). Each stripe measured ¼ of the span of the wall in the perpendicular direction: Vertical (V) stripes were 15 cm wide, while horizontal (H) stripes were 12.5 or 16.25 cm wide depending on the arena (height of 50 or 65 cm, respectively). The panels were arranged in the order V(WBWB), V(BWBW), H(WBWB), H(BWBW), such that each corner provided globally distinct spatial-cue information with respect to stripe orientation (VV, VH, HH, HV) and locally distinct information at the base of the arena with respect to stripe color (BB, WB, BW, WW; Fig. 3a).

Fig. 3.

Diagrams of the arenas and results from Experiment 3 (top row) and Experiment 4 (bottom row). The diagrams (a, d) show flattened views of the featural arenas used in the experiments. In Experiment 3, a cued arena was used in which each wall had a different pattern of vertically or horizontally oriented black-and-white stripes. In addition to the cued arena used in Experiment 3, Experiment 4 also used a scrambled arena in which each wall had an identical pattern of two horizontal stripes at the bottom and four vertical stripes at the top. The graphs show the mean proportion of trials on which rats explored in the place task (b, e) and the object task (c, f). For both tasks, exploration in Experiment 3 is shown separately for each diet group and for each arena condition, and exploration in Experiment 4 is shown for each arena condition. In all graphs, the dashed line indicates chance performance, and the error bars show +1 SEM. HFHS = high-fat, high-sugar.

The scrambled arena contained four identical panels, each horizontally striped in the bottom half (WB from bottom to top) and vertically striped in the top half (BWBW from left to right; see Fig. 3d). Therefore, the scrambled arena provided the same amount of overall spatial-cue information as the cued arena, but did not provide any distinct information at the corners of the arena.

Procedure

In Experiment 3, context familiarization occurred over 2 days immediately before the start of the diet. Rats in both the chow and HFHS groups were tested in the cued and standard arenas. Because all rats were on chow during this time, the standard arena was used for familiarization. This procedure ensured that there were no training benefits from the context-familiarization sessions carrying over to the test sessions if rats had been familiarized to their respective arena conditions, particularly for HFHS rats in the cued-arena condition. In Experiment 4, context familiarization occurred during the diet exposure across Days 2 and 3, to alleviate concerns of potential training effects but allow rats to be familiarized to their respective arena conditions. In this experiment, only HFHS rats were used, but they were tested using the novel-corner variant of the place and object task in the standard, cued, and scrambled arenas. For analysis, place trials were selected equally across between-groups conditions (diet and type of arena in Experiment 3 and type of arena in Experiment 4). All other procedures and testing timelines were the same as in the previous experiments.

Results

In Experiment 3, chow rats had good place-recognition memory in both the standard and cued arenas, as indexed by the high novelty preferences. Critically, HFHS rats tested in the cued arena performed comparably with chow rats and showed a higher novelty preference than HFHS rats tested in the standard arena (Fig. 3b). On the place task, the HFHS group’s performance in the standard arena was significantly lower than that of the other three groups, F(1, 28) = 6.91, p = .014, d = 0.70, who did not differ from each other (using orthogonal contrasts comparing HFHS rats’ performance in the cued arena with chow rats’ performance in the two arenas and comparing the chow group’s performance in each arena against each other, Fs < 1); on the object task, the same set of orthogonal contrasts revealed no significant differences, Fs < 1, except for the contrast comparing the chow group’s performance in each arena, F(1, 14) = 2.12. This result suggests that the addition of spatial cues allowed HFHS rats to encode the location of objects in the arena. However, the cued arena differed from the standard arena in two ways: The walls were more salient, which allowed for easier encoding of spatial information, and each corner was distinct, which provided a landmark for navigation.

In Experiment 4, we used a scrambled arena to break this confound. The scrambled arena defined the walls just as well as the cued arena but did not provide distinctive spatial-cue information at each of the corners. Because chow rats should perform equally well on the scrambled arena as on the standard and cued arenas, we tested rats fed only the HFHS diet in this experiment. The results replicated those of Experiment 3, showing that rats exhibited better place-recognition memory in the cued than in the standard arena. Critically, HFHS rats were impaired in place-recognition memory in the scrambled arena, exhibiting performance comparable with those tested in the standard arena (Fig. 3e). On the place task, performance in the cued arena was significantly higher than performance in the standard and scrambled arenas, F(1, 29) = 14.29, p < .001, d = 0.89, which did not differ from each other, F(1, 20) = 0.11; on the object task, the same set of orthogonal contrasts revealed no significant differences, F(1, 29) = 2.42 and F(1, 20) = 0.28, respectively.

Discussion

The results show that HFHS rats can solve the place task when provided with individuating walls and corners, featural cues that act as landmarks to serve as a reference for encoding location. In contrast, HFHS rats are impaired when required to remember locations in the standard and scrambled arenas. That is, HFHS rats are impaired in the use of spatial information required for the standard and scrambled arenas (geometrical) but not for the cued arena (featural).

Experiment 5

Two types of information can be used for spatial navigation (Cheng, Huttenlocher, & Newcombe, 2013; Spelke & Lee, 2012): geometrical and featural. Geometrical information involves the encoding of displacement and metric properties, including distance, direction, and length information. This type of information is used for mapping the shape of an environment. In contrast, featural information involves the encoding of surface markings and form, including luminance, pattern, and shape information. This type of information is used for positioning landmarks on a map. Evidence that these two types of spatial information can be dissociable comes from studies showing that untrained rats and other vertebrates (including fish, birds, monkeys, and young children) orient themselves using geometry rather than features (Cheng & Newcombe, 2005; Gouteux & Spelke, 2001). These demonstrations have used rectangular environments with distinctively cued walls and corners. Having had a brief exposure to food at one corner, rats subsequently spend equal search time at that (correct) corner and the geometrically symmetrical (diagonally opposite) corner of a rectangular arena, despite the correct location being featurally distinct (Cheng, 1986).

In the current experiment, we tested the hypothesis that an HFHS diet selectively impairs the use of geometrical information by examining place-recognition memory in a rectangular arena. Because geometry prevails over features for orientation, chow rats will confuse diagonally opposite corners in a place-recognition task involving a cued arena. Conversely, if HFHS rats are impaired in the use of geometrical but not featural information, they will not confuse diagonally opposite corners in a cued-arena place task because they can use only featural information.

Method

Subjects

Subjects were 32 rats of the same sex and strain as in the previous experiments. Rats were from the same supplier and were kept under the same conditions. None had performed in previous experiments, and all weighed between 200 and 300 g on arrival.

Apparatus

The place-recognition-memory task was conducted in a rectangular arena (width = 60 cm, length = 90 cm, height = 65 cm). Two versions of the arena—cued and standard—were created. The walls for the standard arena were made of black Perspex. The walls for the cued rectangular arena were similar in design to those used for the cued square arena in Experiments 3 and 4, with two adjacent vertically striped walls and two adjacent horizontally striped walls. Two vertical stripes were added along the vertically striped long wall to fill the increased length while keeping the stripe width the same between experiments. This design held spatial frequency constant between the square and rectangular arenas.

Procedure

In Experiment 5, rats in both the HFHS and chow groups performed the place task in both arena conditions and with objects moved to opposite and adjacent corners. Rats were familiarized, before the start of the diet, to the cued and standard arenas in a counterbalanced order. The rats were also transported on test days in a plastic bucket (diameter = 27 cm, height = 26 cm) with bedding and a lid slightly ajar to allow a small amount of light. They were then placed inside the arena at one of eight starting locations (Cheng, 1986) counterbalanced in a Latin-square design within groups and across tests before repeating with a different Latin-square design. The eight starting locations were facing the center from the north, east, south, and west wall, and conversely, at the center facing the north, east, south, and west wall. These additional steps of bucket transportation and variation in the starting location were to ensure that the rats were disoriented. Experiment 5 also differed in the layout of the objects in the arena (Fig. 4a). During familiarization, one of the two objects was always in the center of the arena, whereas the other was in one of the corners. At test, the corner object had been moved to either a geometrically symmetrical location (the opposite corner) or a geometrically asymmetrical location (an adjacent corner). For analysis, place trials were selected equally across diet and arena conditions. All other procedures were the same as in previous experiments.

Fig. 4.

Design of and results from Experiment 5. Two objects were used in a rectangular arena; one of the objects was placed in the center of the arena and one in the corner. Between familiarization and test (a), the corner object was moved to either a geometrically symmetrical location (the opposite corner) or a geometrically asymmetrical location (an adjacent corner). The graphs show the mean proportion of trials on which rats explored as a function of object movement and group, separately for (b) the standard arena and (c) the cued arena. The dashed lines indicate chance performance, and the error bars show +1 SEM. HFHS = high-fat, high-sugar.

Analysis

Experiment 5 had one exclusion criterion in addition to those used for the previous experiments. Because of the larger arena, rats were less willing to explore the center object during the earlier test trials than in previous experiments. As a result, trials in which a rat explored any object (usually the center one) for less than 1 s in total were excluded to prevent invalidly high exploration ratios. This had never previously occurred in the square arena for the previous experiments.

Results

In a rectangular arena that contained uniformly black walls, when an object was moved to a geometrically symmetrical corner, both chow and HFHS rats showed a low novelty preference. That is, both groups were poor at discriminating the location change. When an object was moved to a geometrically asymmetrical corner, chow rats showed a higher novelty preference than HFHS rats (Fig. 4b). Planned orthogonal contrasts treating the four conditions (Diet × Movement Type) separately revealed that performance of chow rats exposed to asymmetrical movement was significantly higher than that of the other three groups, F(1, 54) = 10.13, p = .002, d = 0.76, who did not differ from each other—chow symmetrical vs. the two HFHS groups, F(1, 40) = 1.46; HFHS groups against each other, F(1, 26) = 1.60.

In the cued rectangular arena, when an object was moved to a geometrically symmetrical corner, chow rats again showed a low novelty preference. That is, they failed to discriminate the location change despite distinctive featural information. Critically, HFHS rats showed a higher novelty preference than chow rats, through their use of the distinctive featural information (Fig. 4c). When an object was moved to a geometrically asymmetrical corner, both chow and HFHS rats showed a high novelty preference. Planned orthogonal contrasts treating the four conditions separately revealed that performance of chow rats exposed to symmetrical movement was significantly lower than that of the other three groups, F(1, 56) = 17.88, p < .001, d = 1.02, who did not differ—chow asymmetrical vs. the two HFHS groups and the HFHS groups against each other, Fs < 1.

Discussion

The results from Experiment 5 confirmed our predictions. As demonstrated in the standard and cued rectangular arena, respectively, HFHS rats were impaired in the use of geometrical information but had intact use of featural information—this resulted in better performance than chow rats in situations of geometrical confusion.

General Discussion

These experiments showed that exposure to an HFHS diet impairs hippocampal-dependent place-recognition memory (Mumby et al., 2002) in rats. The diet had no detectable effect on perirhinal-dependent object-recognition memory (E. A. Murray & Richmond, 2001) in the same rats and in the same environments. Moreover, the hippocampal impairment was present after a few days of exposure to the diet, persisted across tests, and was specific to the use of geometrical information. The selectivity of the impairment to the use of geometrical information shows that the HFHS diet does not result in a general spatial-information-processing deficit, as rats fed this diet remembered the recent location of objects when provided with featural cues. Rather, it suggests that the diet rapidly results in a processing deficit specific to distance and direction information.

Solving the place task requires recognizing that one of the two objects has moved to a new location. In the standard (and scrambled) arena consisting of indistinct walls, place recognition relies on having one coordinate to position each object onto a cognitive map of the arena. These coordinates could be vectors containing distance and direction information, such as distance to a wall and heading direction (Cheng, 1989; Collett, Cartwright, & Smith, 1986). Good recognition memory, therefore, would include one coordinate for each object representing its distance and direction to the edge of the arena; each coordinate could be a single vector to the corner, two vectors to the walls, or a combination of both vector-to-edge types (Fig. 5a). These coordinates, however, are confusable relative to any one of four frames of reference taken up by each of the walls. In contrast, coordinates in the cued arena consisting of distinctively cued walls and corners are unambiguous, as the featural information provides a single frame of reference.

Fig. 5.

Diagrams illustrating the place-based vector model in the standard arena (with indistinct walls) and the view-based matching model in the cued arena (with distinct walls). In the flattened representation of the standard arena (a), arrows represent vectors containing distance and direction information for positioning the objects onto a cognitive map of the arena. The length of the arrow represents the distance information; the angle relative to a wall represents the direction information. One object can be represented by a single coordinate (x1), and the other object can be represented by two coordinates (y1, y2). In the flattened representation of the cued arena (b), the solid arrow represents a change in the location of one of the objects; broken arrows represent different viewpoints from the center of the arena (v1, v2). The 3-D view of the cued arena (c) shows that when the object is moved, its background when viewed from the center of the arena changes.

Alternatively, a view-based matching (taxon) strategy could be adopted in the cued arena instead of a place-based vector (locale) strategy used for positioning objects onto a cognitive map (O’Keefe & Nadel, 1978; Sheynikhovich, Chavarriaga, Strösslin, Arleo, & Gerstner, 2009). According to this view-based strategy, a change in location is also accompanied by a change in background featural cues (Figs. 5b and 5c). Therefore, rats fed the HFHS diet either (a) cannot position coordinates onto a vector space under situations of high load or confusability, such as when there are multiple frames of reference, or (b) cannot compute or integrate distance and direction information into a coordinate, which requires them to employ taxon-based strategies for spatial learning and memory. In either case, the HFHS diet impairs the use of geometrical information used in locale-based strategies required for the formation of a cognitive map.

This explanation of the diet-induced deficit in spatial geometry and locale navigation can be grounded in neurophysiology. Neurons in the rat hippocampus exhibit distinct firing patterns corresponding to different locations of an environment; these place cells are thought to be the neural basis for a cognitive map (O’Keefe, 1976). Electrophysiological recording from place cells during place-recognition tasks have shown that (a) place cells fire more to familiar objects in a novel location than to novel objects in a familiar location (Manns & Eichenbaum, 2009) and (b) place-cell firing during exploration of a familiar object in a novel location is not spatially localized (Larkin, Lykken, Tye, Wickelgren, & Frank, 2014). This lack of localized firing at old or novel locations in the arena suggests that objects encountered are not encoded as points of interest on an existing cognitive map. Rather, place-cell firing may represent objects on a cognitive map by encoding their spatial relationship to the environment. Although speculative, this theory makes place cells—and adjunct neural spatial mechanisms such as boundary-vector cells (Lever, Burton, Jeewajee, O’Keefe, & Burgess, 2009; Solstad, Boccara, Kropff, Moser, & Moser, 2008), head-direction cells (Taube, Muller, & Ranck, 1990), and grid cells (Hafting, Fyhn, Molden, Moser, & Moser, 2005; Moser, Kropff, & Moser, 2008)—potential candidates for the neural mechanism underlying the vector-coordinate model described for solving the place task. Thus, this hypothesis implies that the HFHS diet impairs place-recognition memory by disrupting functioning of hippocampal place cells or boundary, directional, and grid cells.

The present findings may have implications for dietary effects in people. First, our results point to a selective impairment in hippocampal-dependent function. Notably, the same pattern of results as those found in Experiment 5 has been shown in individuals with Williams syndrome, which is characterized by severe and selective impairment of spatial ability (Wang, Doherty, Rourke, & Bellugi, 1995). As in the HFHS rats, individuals with Williams syndrome were impaired in the use of geometry but performed well in featurally distinct environments and did not show geometric confusion in a reorientation task (Lakusta, Dessalegn, & Landau, 2010). These results show that damage to human hippocampal and surrounding parietal areas stemming from a genetic abnormality (Meyer-Lindenberg et al., 2004; Meyer-Lindenberg et al., 2005) can impair the ability to use geometrical information. Second, our results showing diet-induced impairments in geometric processing provide an explanation for why HFHS intake in adolescents predicts worse performance on a spatial problem-solving task (Nyaradi et al., 2014) and self-reported difficulties in mathematics, even after controlling for social and health factors (Overby et al., 2013). Furthermore, greater body weight in this age group has also been shown to independently predict worse visuospatial organization (Li et al., 2008). Therefore, a well-balanced diet may be critical for appropriate development of spatial ability, particularly in younger children, who primarily rely on geometrical information for spatial navigation (Gouteux & Spelke, 2001).

Finally, the present results combine with previous findings (Beilharz et al., 2014; Kanoski & Davidson, 2010; A. J. Murray et al., 2009) to show that a modern-style diet impairs hippocampal-dependent cognitions well in advance of effects on body weight. However, the hippocampus is involved not only in various forms of cognitions, but also in monitoring the internal milieu and regulation of feeding and energy balance (Carlini et al., 2004; Davidson et al., 2009; Parent, Darling, & Henderson, 2014). For example, lesions to and functional inactivation of the hippocampus disrupt aspects of hunger signaling (see Parent et al., 2014) and the inhibitory processes required for solving discrimination problems (see Kanoski & Davidson, 2011). Together, these findings have led to the proposal that a vicious cycle contributes to obesity, whereby overconsumption of foods rich in fats and sugars impairs hippocampal functioning, which in turn dysregulates feeding behaviors to further increase energy intake (Kanoski & Davidson, 2011; Parent et al., 2014).

Footnotes

Acknowledgements

The authors thank Ehsan Arabzadeh, Ken Cheng, Elizabeth Spelke, and Nathan Holmes for helpful comments, and Anna Holtby, Belinda Lay, Nathan Han, and Robyn Winwood-Smith for assistance with scoring.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interest with respect to their authorship or the publication of this article.

Funding

D. M. D. Tran was funded by an Australian Postgraduate Award and a Brain Sciences University of New South Wales PhD Top-Up scholarship.

Supplemental Material

Additional supporting information can be found at

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